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Web Topic 7.5
Adaptations for passive electroreception

Introduction

The early acquisition of passive electroreceptors in primitive fish was surely a key adaptation that facilitated its subsequent radiation and eventual dominance in aquatic habitats. In both marine and freshwater habitats, a number of strategies are employed to enhance passive electroreception.

Variations in the spatial distribution of receptors

Spreading many ampullary organs (or teleost equivalents) over a large area of body surface allows an animal to sample the amplitude of the electric field at many locations. Because the walls of ampullary canals are highly resistive, little current passes into or out of the canal except along its major axis. Thus electric field lines parallel to a canal will produce the largest stimulation of the associated sensory cells. Comparisons of stimulus levels for canals with nearby pores but different axis angles thus allow the animal to estimate not only the strength of the electrical field at a location but also its direction there. Pooling of inputs from many organs then permits the animal’s brain to generate a fairly accurate map of the electrical field surrounding the sampled body surface (Montgomery and Bodznick 1999; Brown 2002; Keller 2004; Bell and Maler 2005; Bodznick and Montgomery 2005). This map can be extremely useful in determining the location of the electric field source and whether it is moving relative to the sampling animal.

Whereas lampreys, lungfish, and several extinct taxa of primitive fish spread their electroreceptive organs over much of their body surface (Bodznick and Northcutt 1981; Northcutt 1986; Ronan 1986; Northcutt 1997; Watt et al. 1999), the majority of passively electroreceptive animals concentrate them in relevant regions of their heads (Northcutt 1986; Zakon 1988; Jørgensen 2005). Within the head region, the distribution of the organs and their associated pores varies with the species’ habitat, diet, and light levels when foraging. Because ampullary organs develop from the same embryonic tissues as the lateral line, their distribution is also affected by the disposition of the animal’s hydrodynamic canals and superficial neuromasts (Northcutt 1986).

The 400–2500 ampullary receptors of sharks are concentrated entirely on their heads (Bodznick and Boord 1986). Species that forage in open ocean tend to have a more even distribution of receptors over the head’s dorsal and ventral surfaces while those that forage on benthic prey (such as skates) concentrate the receptors on the ventral side particularly around the mouth (Tricas 2001; Collin and Whitehead 2004). Sharks that feed on benthic prey as juveniles but in deeper waters as adults undergo a shift towards more even dispersion of ampullary receptors as they mature (Collin and Whitehead 2004). A more widespread distribution of receptors on the head would also facilitate the use of the earth’s electric fields for migratory species, but whether sharks can actually use electroreception for long range navigation remains unclear (Kalmijn 1974, 1988; Klimley 1993; Paulin 1995; Sundstrom et al. 2001; Collin and Whitehead 2004; Tricas and Sisneros 2004; Wilkens and Hofmann 2005).

Figure 1. Distribution of ampullary organ pores on the heads of sharks as function of foraging habitats. Ventral view (left half), dorsal view (right half), and ampullary canal openings (dots) are shown in each example. A) Hammerheaded sharks (Sphyrna spp.) often feed just over the bottom of bays and estuaries, and young sharks live in murky waters with low visibility. Approximately 60% of their canal openings are on the ventral side of their bodies where prey are more likely to be encountered. B) Sandbar sharks (Carcharhinus plumbeus), like most shark species, have equal numbers of ampullary canal openings on the ventral and dorsal sides of the head. They encounter prey both above and below the body and can use vision to orient their attacks. C) Bull sharks (Carcharinus leucas) are unusual in their ability to tolerate brackish and freshwater habitats with limited visibility. Like the hammerheaded sharks, bull sharks concentrate nearly 60% of their ampullary canal openings on their ventral side ahead of and to the side of their mouth. (After Collin and Whitehead 2004.)

The head of a skate or a ray merges smoothly into the flattened wings on each side of the body. Adult skates and rays can have from 400–1400 ampullary organs depending on the species (Bodznick and Boord 1986). These are usually clustered around the head but radiate their canals in all directions including several long canals that open on the rear edges of the wings. As with sharks, species that feed on benthic prey have higher concentrations of receptors and canal pores on their ventral side and around the mouth, whereas larger species that pursue fish as prey have a more even distribution on the dorsal and ventral sides of their bodies (Bodznick and Boord 1986; Raschi 1986; Tricas 2001). Large pelagic species, such as the manta rays (Myliobatidae), have many fewer electroreceptors than shallow water forms and these are limited to small patches on their ventral side (Bodznick and Boord 1986).

Freshwater paddlefishes (Polyodontidae) feed on tiny (< 5mm) planktonic crustaceans such as Daphnia. Each fish sports a long flat rostrum on its head:

Figure 2. Photo of paddlefish (Polyodon spathula) foraging with mouth open. Paddle extends forward from head. (Photo by David Alexander.)

This rostrum is covered with up to 75,000 ampullary organs (Wilkens et al. 1997; Wilkens et al. 2001) that allow the fish to detect the passive electric fields of their tiny prey at distances of up to 10 cm and respond by turning appropriately and engulfing the crustaceans in their widespread mouths (Russell et al. 1999; Russell et al. 2001; Wojtenek et al. 2001; Wilkens 2004).

Figure 3. Distribution of ampullary organs on dorsal side of paddlefish rostrum (paddle). Rostrum attaches to remainder of head on right of figure. (After Wilkens 2004.)

Sturgeons (Acipenseridae), close relatives of the paddlefish, concentrate their ampullary organs and canals on the ventral side of their heads (Teeter et al. 1980; Gibbs and Northcutt 2004). While both freshwater and marine catfish (Siluriformes) distribute ampullary-like receptors over their entire bodies (including the caudal fin), they also have the greatest concentrations on their heads and especially around their eyes (Peters and Meek 1973; Finger 1986; Northcutt et al. 2000). Interestingly, catfish barbels appear to function only as chemoreceptive and tactile organs and completely lack electroreceptors. The other teleost fish with ampullary-like receptors, the knifefish, elephantfish, featherbacks, and frankfish, all concentrate these organs on the head with a gradient of decreasing density as one moves towards the tail (Zakon 1986; Jørgensen 2005).

A foraging platypus uses a similar array of passive electroreceptors on its bill to detect nearby shrimp, leeches, and other freshwater invertebrates (Scheich et al. 1986; Manger and Pettigrew 1995; Pettigrew et al. 1998; Pettigrew 1999). Both marine and freshwater catfish (Siluriformes) combine inputs from ampullary, hydrodynamic, and olfactory organs to detect, track, and capture their prey (Roth 1972; Kalmijn 1974; Finger 1986; Peters et al. 1999; Lorteije et al. 2000; Pohlmann et al. 2004), and North American catfish (Ictaluridae) may use their ampullary-like organs to navigate and identify specific locations using local electrochemical fields (Peters and Bretschneider 1972; Kalmijn 1974; Peters and Vanwijla.F 1974; Finger 1986; Kalmijn 1988). Some freshwater catfish may also use passive electroreception to localize and interact with conspecifics in a manner similar to that of marine stingrays (Peters et al. 2002).

In all of these species, the emphasis on passive electroreceptive organs in only one part of the body is surely a result of the limited range over which these stimuli can be detected. Given that most animals are moving in an anterior direction and that passive electroreception is most widely used to detect prey, concentrating the receptors in the anterior end of the animals would seem the logical strategy.

Variations in the frequency tuning of receptors

Another strategy for improving passive electroreception is to tune the maximal responsiveness of the passive electroreceptors to the frequency range of those electric fields that are of greatest interest to the animal. In many cases, the optimal frequencies are those generated by ventilation and locomotion of conspecifics or the animal’s prey. In addition to increasing sensitivity to desired stimuli, narrow frequency tuning also excludes irrelevant electrical fields that otherwise would be detected and constitute noise. Although some animals specialize in detecting relatively invariant electrical fields, even these species are most sensitive to stimuli whose amplitudes are at least slightly time-variant. For example, frequencies as low as 0.03–1 Hz will elicit responses in stingrays and catfish, whereas these same animals will ignore a steady field of similar amplitude if neither they nor the source are moving (Finger 1986; Tricas and New 1998; Peters et al. 1999; Tricas and Sisneros 2004). This preference for slightly varying fields is probably due to the fact that there is nearly always some relative motion between the sensing animal and the source of the electrical field. This will transform what the animal perceives from a steady field into a slowly varying one (Hofmann and Wilkens 2005). Because sharks routinely sway their heads left and right as a result of their swimming style, they experience a steady electric field as one that varies in amplitude at a rate of about 1 Hz (Kalmijn 1988). The ampullary receptors of sharks thus require stimuli that vary temporally by at least 1–2 Hz. Rays and skates also favor low frequency stimuli in the range of 0.5–2 Hz (Tricas and Sisneros 2004). Other taxa tend to focus on higher frequencies for passive electroreception: optimal frequency ranges are 2–7 Hz for paddlefish, 6–12 Hz for catfish, 30–50 Hz for knifefish and elephantfish, and 50–100 Hz for the platypus (Zakon 1988; Wilkens 2004; Bodznick and Montgomery 2005).

Acknowledgements

We thank David Alexander (https://www.flickr.com/search/?text=Davidalexander) for use of the paddlefish photo.

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